SciELO - Scientific Electronic Library Online

 
vol.87 número3Lista de los helmintos parásitos de primates silvestres de BrasilDescripción de la genitalia de Coptocycla (Psalidonota) leprosa (Chrysomelidae: Cassidinae: Cassidini) índice de autoresíndice de assuntospesquisa de artigos
Home Pagelista alfabética de periódicos  

Serviços Personalizados

Journal

Artigo

Indicadores

Links relacionados

  • Não possue artigos similaresSimilares em SciELO

Compartilhar


Revista mexicana de biodiversidad

versão On-line ISSN 2007-8706versão impressa ISSN 1870-3453

Rev. Mex. Biodiv. vol.87 no.3 México Set. 2016

http://dx.doi.org/10.1016/j.rmb.2016.06.009 

Taxonomía y sistemática

Macroparasites of silversides (Atherinopsidae: Odontesthes) in Argentina

Macroparásitos de pejerreyes (Atherinopsidae: Odontesthes) en Argentina

Verónica Floresa  * 

Liliana Semenasa 

Carlos Rauquea 

Rocío Vegaa 

Valeria Fernandeza 

María Lattucab 

a Laboratorio de Parasitología, Instituto de Investigaciones en Biodiversidad y Medioambiente del Consejo Nacional de Investigaciones Científicas y Técnicas - Universidad Nacional del Comahue, Quintral 1250, 8400 Bariloche, Río Negro, Argentina

b Laboratorio de Ecofisiología, Centro Austral de Investigaciones Científicas (CADIC-CONICET), Bernardo Houssay 200, V9410BFD Ushuaia, Tierra del Fuego, Argentina

Abstract:

This study presents new geographical distribution records for the macroparasites of the marine Odontesthes nigricans (Richardson, 1848) (89 wild specimens), and for the freshwater silversides Odontesthes bonariensis (Valenciennes, 1835) (43 wild and 108 cultured specimens), and Odontesthes hatcheri (Eigenmann, 1909) (183 wild specimens) from Argentina. These data represent records of 12 parasite taxa for O. nigricans, 8 for O. bonariensis, and 19 for O. hatcheri, which include digeneans, monogeneans, cestodes, nematodes, acantocephalans, mollusks, copepods, and branchiurans. For cultured O. bonariensis, the records of the present study correspond to the first reports of parasites in the literature. This work provides also data on site of infection, parasite load, and development stages for the parasite species.

Keywords: Odontesthes nigricans; Odontesthes bonariensis; Odontesthes hatcheri; Parasites; Argentina; Freshwater; Marine; Wild; Cultured

Resumen:

Este estudio presenta nuevos registros de distribución geográfica de macroparásitos del pejerrey marino Odontesthes nigricans (Richardson, 1848) (89 especímenes silvestres), de los pejerreyes de agua dulce Odontesthes bonariensis (Valenciennes, 1835) (43 ejemplares silvestres y 108 cultivados) y de Odontesthes hatcheri (Eigenmann, 1909) (183 especímenes silvestres) en Argentina. Doce taxones parásitos se registraron para O. nigricans, 8 para O. bonariensis y 19 para O. hatcheri, incluyendo digéneos, monogéneos, cestodos, nematodos, acantocéfalos, moluscos, copépodos y branquiuros. Para los ejemplares de O. bonariensis de cultivo, los registros del presente estudio corresponden a los primeros sobre parásitos en la literatura. Además, se presentan datos sobre la localización del parásito, sus valores de infección y sus estados de desarrollo.

Palabras clave: Odontesthes nigricans; Odontesthes bonariensis; Odontesthes hatcheri; Parásitos; Argentina; Agua dulce; Marinos; Silvestres; De cultivo

Introduction

The species of Odontesthes (silversides) compose the most representative genus of Atherinopsidae, containing 19 species (Dyer, 2006). The silversides have great adaptability to different habitats and are distributed in marine, brackish, and freshwater environments (Dyer, 2006). Due to the flavor of the meat, these fishes are important in recreational fishery, commercial exploitation, and aquaculture (Grosman, 2001). Odontesthes bonariensis (Valenciennes, 1835) is the only cultured species, and has been widely used for repopulation purposes and have been introduced into Europe, Asia, and Africa (Tombari & Volpedo, 2008).

In Argentina, studies on freshwater silversides are mainly focused on culture, genetics, physiology, and ecology of O. bonariensis (Colautti, Garcia, Balboni, & Baigún, 2010; Grosman, 2001), and of Odontesthes hatcheri (Eigenmann, 1909) (Ruiz, 2007). The information on the marine silversides is limited, based mainly on Odontesthes nigricans (Richardson, 1848) and focused on the physiology of the specimens (Lattuca et al., 2009).

Although silversides species are widely distributed, reports of parasites from wild fishes are scarce and scattered (Carballo, 2008; Carballo, Laurenti, & Cremonte, 2011; Carballo, Navone, & Cremonte, 2011; Carballo, Cremonte, Navone, & Timi, 2012; Drago, 2012; Mancini, Rodríguez, Prosperi, Salinas, & Bucco, 2006; Mancini et al., 2008; Ortubay, Semenas, Úbeda, Quaggiotto, & Viozzi, 1994). Besides publications on rearing silversides, there is no published information on their parasites (Tanzola, Semenas, & Viozzi, 2009). The objective of the present work is to report the macroparasite fauna of the wild marine O. nigricans and the wild freshwater O. bonariensis and O. hatcheri, and the cultured O. bonariensis.

Materials and methods

A total of 89 O. nigricans were collected from 2 marine sites, 151 O. bonariensis were collected from 5 sites, and 183 O. hatcheri were collected from 13 sites, both the latter from freshwater environments (Fig. 1; Table 1). The fish were captured using gill and seine nets. Cultured O. bonariensis were collected from outdoor man-made ponds and indoor fiberglass tanks located within the campus of INTECH (Instituto Tecnológico de Chascomús), which were supplied with underground waters, and from floating cages located in Lacombe and Chascomús Pampean Lakes (Fig. 1; Table 1). Specimens of O. hatcheri and O. bonariensis were transported fresh to the laboratory, and those of O. nigricans were slit opened and fixed in 5% formalin in the field. Fish were measured, and necropsied to examine fins, skin, eyes, gills, and all internal organs with the aid of a dissecting microscope. The parasites were collected, identified, and counted. Prevalence and mean intensity were calculated. New geographical record refers to the first date that a parasite is reported in a new biogeographic region, ecoregion or basin, and new host record refers to the first time that a parasite is cited for a new host species. Furthermore, we followed the classification proposed by Niewiadomska (2002) for the family Diplostomidae, who considered as valid the genera Diplostomum, Austrodiplostomum, Tylodelphys, and Dolichorchis. Measurements of specimens are given in μm. Voucher specimens of parasites were deposited in the Colección Helmintológica del Museo de La Plata, Argentina.

Figure 1 Location of the sampling sites of the silversides and their geographical coordinates in Argentina. 

Table 1 Data of silversides, localities of collections, sample, date and size; § cultured fish. 

Host Localities Sample date Sample size Standard fish size (cm)
        Mean Range
O. nigricans Punta María Nov. 2010 67 16.8 9-25
Varela Bay Sep. 2010      
  Jan. 2011 22 22.1 18-25
  Mar. 2011      
O. bonariensis La Plata River Sep. 2011 11 18.5 10-27
Man-made Pond (INTECH) § Nov. 2007 10 11.4 9-16
Chascomús Pampean Lake§ Mar. 2008 77 10.3 8-14
Chascomús Pampean Lake Mar. 2008 32 14.6 9-24
Lacombe Pampean Lake§ Nov. 2007 21 14 13-15
Marimenuco Reservoir Mar. 2001 7 14.0 3-31
Neuquén River Oct. 2011 5 26.7 24-30
Piedra del Águila Reservoir Feb.1999 1 38.0 38
Caleufu River Mar. 2006 3 7.0 6-8
Pond in Villa la Angostura Jan. 2007 2 2.7 2-3
Carrilafquen Lake Oct. 2005 10 21.1 20-22
O. hatcheri Carrilafquen Chica Lake Oct. 2004 58 14.6 8-30
  Aug. 2005      
Morenito Lake Feb. 1999 10 25.4 17-31
  Nov. 2000      
Moreno Oeste Lake Mar.1999 16 31.1 28-36
  Aug. 2000      
Lezana Lake Dec.2010 31 6.9 6-9
  Jan.2011      
Epuyen Lake Mar.2003 3 25.3 22-27
Rivadavia Lake Feb. 2011 27 12.8 6-18
Musters Lake Oct. 2012 10 29.8 27-32

Results

The data obtained represent 15 new geographical records and 2 new host records for O. nigricans (Fig. 2; Table 2); 2 new geographical records, 1 new host record (T. cardiophilus), and a new species (Gyrodactylus sp.) for O. bonariensis (Fig. 3; Table 3); and 24 new geographical records and 1 new host record (Steganoderma szidati) for O. hatcheri (Fig. 4; Table 4). Prevalence and mean intensity for each parasite species, which include digeneans, monogeneans, cestodes, nematodes, acantocephalans, mollusks, copepods and branchiurans, are given in Tables 2,3,4.

Figure 2 Microphotographs of Odontesthes nigricans parasites. 1, Diplostomum sp.; 2, Lecithaster sp.; 3, Proctotrema bartolii; 4, anterior end of Acuariinae sp.; 5, posterior end of Acuariinae sp.; 6, anterior end of Cosmocephalus sp.; 7, posterior end of Cosmocephalus sp.; 8, anterior end of Contracaecum sp.; 9, posterior end of Contracaecum sp.; 10, anterior end of Hysterothylacium sp.; 11, posterior end of Hysterothylacium sp.; 12, anterior end of Cucullanus sp.; 13, posterior end of a Cucullanus sp. female; 14, posterior end of a Cucullanus sp. male; 15, forebody of Hypoechinorhynchus sp.; 16, Corynosoma sp.; 17, Caligus sp.; 18, Peniculus sp. 

Table 2 Parasites of Odontesthes nigricans with data on site of infection, parasitic stage, localities, prevalence (P), mean intensity (MI), voucher specimens (VS), and collection number (CN). A, adult; C, Cysthacanth; L3, Larva 3; M, Metacercaria. *New geographical record; ¥new host record; §cultured fish. 

Parasite Site Stage Locality P (%) MI VS-CN
Diplostomum sp.¥ Lens M Varela* 8.6 8.0 MLP-He 7125
Lecithaster sp. Intestine A Varela* 30.0 11.6 MLP-He 7126
Proctotrema bartolii Intestine A Punta María* 48.4 16.5 MLP-He 7127
Acuariinae gen. et sp.¥ Liver and abdominal cavity L3 Punta María* 12.9 1.8 MLP-He 7128
      Varela 15.7 1.9  
Cosmocephalus sp. Liver and abdominal cavity L3 Punta María* 9.7 4.0 MLP-He 7129
      Varela* 8.6 1.6  
Contracaecum sp. Abdominal cavity L3 Varela* 1.4 1.0  
Hysterothylacium sp. Intestine L3 Punta María 3.2 1.0 MLP-He 7130
Cucullanus sp. Intestine A Varela* 2.9 1.0  
Hypoechinorhynchus sp. Intestine A Varela* 2.9 1.5 MLP-He 7131
      Punta María* 9.7 4.0  
Corynosoma sp. Mesenteries, liver C Varela* 7.1 1.0 MLP-He 7132
      Punta María* 35.5 3.4  
Caligus rogercresseyi Dorsal, caudal fins A Varela* 11.4 1.8 MLP-Cr 27001
      Punta María* 29.0 1.0  
Peniculus sp. Body surface, fins A Varela* 28.6 5.3 MLP-Cr 27002

Figure 3 Microphotographs of Odontesthes bonariensis parasites. 19, Tylodelphys cardiophilus; 20, Gyrodactylus sp.; 21, escolex of Cangatiella macdonaghi; 22, proglotids of Cangatiella macdonaghi

Table 3 Parasites of Odontesthes bonariensis with data on site of infection, stage, localities, prevalence (P), mean intensity (MI), voucher specimens (VS), and collection number (CN);§cultured fish; A, adult; L3, Larva 3; M, Metacercaria. *New geographical record; ¥new host record. 

Parasite Site Stage Locality P (%) MI VS-CN
Austrodiplostomum mordax brain M Lacombe§ 100 13.8  
Tylodelphys cardiophilus ¥ pericardic cavity M Lacombe§* 28.5 1.3 MLP-He 7133
Ascocotyle sp. heart M Chascomús§ 42.9 3.3
  Chascomús 31.3 10.6
Phagicola sp. gills M Chascomús§ 5.2 2.0
Gyrodactylus sp. gills and fins A fiberglass tanks 28.6 6.7 MLP-He 7134
man made pond 60.0 3.4
Chascomús§ 90.5 4.5
Chascomús 31.3 10.6
Cangatiella macdonaghi intestine A Lacombe§ 85.7 13.8
Chascomús§ 10.4 9.1 MLP-He 7135
Chascomús 96.9 66.7
Contracaecum sp. abdominal cavity L3 La Plata River 9.1 1.0
Lacombe§ 14.3 1.7
Chascomús§ 3.9 1.0
Chascomús 25.0 1.6
Argulus sp. tegument A Lacombe§* 4.7 1.0

Figure 4 Microphotographs of Odontesthes hatcheri parasites. 23, Austrodiplostomum mordax; 24, Steganoderma macrophallus; 25, Steganoderma szidati

Table 4 Parasites of Odontesthes hatcheri with data on site of infection, stage, localities, prevalence (P), mean intensity (MI), voucher specimens (VS), and collection number (CN); A, adult; G, Glochidium; L3, Larva 3; M, Metacercaria. *New geographical record; ¥new host record. 

Parasite Site Stage Locality P (%) MI VS-CN
Austrodiplostomum mordax Brain M Carrilafquen Chica 50 6.3 MLP-He 7136
      El Chañar 60 5.0  
      Marimenuco 14.3 41.0  
Diplostomum sp. Eyes M Musters 80 80.5  
Tylodelphys barilochensis Brain M Moreno 5.9 1.0  
             
Tylodelphys cardiophilus Pericardiccavity M Carrilafquen Chica 3.8 1.0 MLP-He 7137
Tylodelphys destructor Brain M Carrilafquen Chica 17.0 1.0 MLP-He 7138
      El Chañar 40.0 2.0  
Tylodelphys barilochensis Brain M Morenito 6.3 4.0  
      Epuyén 66.6 3.0  
      Lezana 22.6 4.6  
      Marimenuco 14.3 4.0  
             
             
Stephanoprora uruguayense Gills M El Chañar 100.0 57.4  
      Marimenuco 42.9 2.3  
Steganoderma macrophallus Intestine A El Chañar 40.0 2.0 MLP-He 7139
      Musters 30.0 224.0  
Steganoderma szidati Intestine A Moreno 5.9 40.0 MLP-He 7140
Cangatiella macdonaghi Intestine A El Chañar 80.0 10.8  
      Marimenuco 57.1 4.5  
      Morenito 43.8 20.3  
      Moreno 64.7 27.7  
      Musters 30.0 9.6  
Contracaecum sp. Intestinewall L3 El Chañar 20.0 2.0  
      Carrilafquen Chica 3.8 1.0  
      Morenito 6.3 1.0  
      Moreno 23.5 1.3  
      Musters 40.0 2.0  
      Caleufu 33.3 1.0  
Hysterothylacium patagonense Intestine L4 Morenito 6.3 3.0  
      Moreno 23.5 5.8  
      Epuyen 33.3 1.0  
Camallanus corderoi Intestine A Marimenuco 42.9 1.3  
      Morenito 31.3 18.8  
      Moreno 47.0 12.1  
      Lezana 3.2 1.0  
      Musters 10.0 3.0  
Acanthocephalus tumescens Intestine A Carrilafquen Chica 14.3 3.7  
      Morenito 6.3 2.0  
      Rivadavia 11.1 3.7  
Pomphorhynchus patagonicus Intestine A Lezana 3.2 1.0  
      Musters 90.0 12.8  
Diplodon chilensis Gills,fins G Carrilafquen 28.6 2.8  
      Morenito 12.5 28.5  
      Moreno 58.8 35.9  
      Epuyen 100.0 13.6  
      Rivadavia 22.2 2.8  
Ergasilus sieboldi Gills A Marimenuco 42.9 2.3  
      El Chañar 40.0 3.0  
      Piedra del Águila 100.0 2.0  
      Morenito 56.3 6.0  
      Moreno 88.2 19.7  
      Musters 100.0 46.0  

The marine silverside, O. nigricans, was parasitized by the digeneans Diplostomum sp., Lecithaster sp., Proctotrema bartolii Carballo, Laurenti, & Cremonte, 2011. The following nematodes Acuariinae gen. et sp., Cosmocephalus sp., Contracaecum sp., Hysterothylacium sp. and Cucullanus sp., the acanthocephalans Hypoechinorhynchus sp. and Corynosoma sp., and the copepods Caligus rogercresseyi (Boxshall & Bravo, 2000) and Peniculus sp. were also recorded (Table 2). The specimens of Diplostomum were assigned to this genus since they are metacercariae of the “Diplostomulum” type (not encysted metacercariae), which were localized in the lens of fish. The metacercariae measured 260-701 in length × 144-326 width, had the anterior end of the body trilobate, with small lateral protuberances (lappets) on either side of the oral sucker (36-72 long × 36-65 wide); the ventral sucker (26-72 long × 29-65 wide) was located postequatorially and is similar in size to that of the oral sucker. Just behind the ventral sucker there is a longitudinal holdfast organ (65-168 long). The specimens of Lecithaster sp. collected presented a 4-lobed ovary and a vitellarium rosette-shaped with 7 lobes. The larvae 3 of Acuariinae gen. et sp. have well developed pseudolabia, but the lateral alae are absent, therefore they could not be assigned to any known genus. The Cucullanus specimens collected in this study (1 male and 2 immature females) have the deirids located in the first third of the esophagus (182-193 from the anterior end), absence of papillae anterior to ventral sucker, presence of gubernaculum, and spicules reaching anterior end of ventral sucker. Peniculus sp. have a cephalothorax of 454 long × 511 wide; a neck of 227-284 long, a trunk 3,550-4,658 long × 880-1,227 wide, a ratio length to wide trunk of 3.6-4.0, with 4 swimming legs, with 3 and 4 further apart from legs 1 and 2.

The freshwater silverside O. bonariensis was parasitized by metacercariae of Austrodiplostomum mordax Szidat and Nani, 1951, Tylodelphys cardiophilus Szidat, 1969, Ascocotyle sp., and Phagicola sp., the monogenean Gyrodactylus sp., the cestode Cangatiella macdonaghi (Szidat & Nani, 1951), the nematode Contracaecum sp., and the branchiuran Argulus sp. (Table 3). Odontesthes hatcheri was parasitized by the digeneans A. mordax, Diplostomum sp., Tylodelphys barilochensis Quaggiotto and Valverde, 1992, T. cardiophilus, Tylodelphys destructor Szidat and Nani, 1951, Ascocotyle sp., Phagicola sp., Stephanoprora uruguayense Holcman-Spector and Olagüe, 1989, Steganoderma macrophallus Szidat and Nani, 1951, and Steganoderma szidati Viozzi, Flores and Ostrowski de Núñez, 2000, the cestodes C. macdonaghi, the nematodes Contracaecum sp., Hysterothylacium patagonense Moravec, Urawa and Coria, 1997, and Camallanus corderoi Torres, Teuber and Miranda, 1990, the acanthocephalans Acanthocephalus tumescens (von Linstow, 1896) and Pomphorhynchus patagonicus Ortubay, Úbeda, Semenas and Kennedy, 1991, the mollusk Diplodon chilensis Gray, 1828 and the copepod Ergasilus sieboldi von Nordman, 1832 (Table 4). As mentioned above, the metacercariae collected from the lens of O. hatcheri, which were the diplostomulum type were assigned to the genus Diplostomum. They measured 509-701 in length × 259-336 width. They also had the anterior end of the body trilobate, with small lateral lappets on either side of the oral sucker (53-82 long × 48-72 wide); the ventral sucker (36-60 long × 43-60 wide) is oval to round, located postequatorially and similar in size to that of the oral sucker. Just posterior to ventral sucker is the holdfast organ (96-144 long).

For cultured O. bonariensis, the parasite richness was 1 parasite species (Gyrodactylus sp.) taken from samples from indoor fiberglass tanks, and for those cultured outdoor in man-made ponds, 5 species (A. mordax, T. cardiophilus, C. macdonaghi, Contracaecum sp., and Argulus sp.) for fish reared in cages of Lacombe Pampean Lake, and also 5 species (Ascocotyle sp., Phagicola sp., Gyrodactylus sp., C. macdonaghi, and Contracaecum sp.) for those collected from cages of Chascomús Pampean Lake (Table 3).

Discussion

Specimens belonging to Digenea, Monogenea, Cestoda, Nematoda, Acanthocephala, Mollusca, Copepoda, and Branchiura are reported herein. Since larvae were the most common stages found in previous as well as, in the present work, the taxonomic identification at species level is difficult, considering that many of these parasites and their life cycles are not yet elucidated. All records reported in this study represent 41 new geographical records, 4 new host records and 1 new parasite species.

For O. nigricans, the parasites Diplostomum sp. and Acuariinae gen. et sp. were reported for the first time, and Cucullanus sp. may be a new parasite species. With regard to the Diplostomum metacercaria, we assumed that the metacercariae of O. nigricans and O. hatcheri belong to the same species as they show similar morphometric characteristics. Diplostomum species that have been found in the Antarctic region are D. minutum Szidat, 1964; D. antarcticum Freiler, 1986; and D. dominicanum Freiler, 1986 recorded from the kelp gull Larus dominicanus (González-Acuña et al., 2009). The metacercariae of Diplostomum found in O. nigricans and O. hatcheri could possibly correspond to D. minutum since adults of this species have been reported in L. dominicanus in Chubut and in Antarctica (Niewiadomska, Zdzitowiecki, & Ostrowski-de Núñez, 1989), near the site of the present study. It has been pointed out that lens metacercariae of Diplostomum have a low specificity (Locke et al., 2015), so the marine silverside could be infected with cercariae of Diplostomum when they ascend the rivers in the Magellan Strait (Dyer, 2000).

Lecithaster australis Prudhoe and Bray, 1973 and L. micropsi Zdzitowiecki, 1992 were recorded in several species of nothotenids and gadiids in the South West Atlantic Ocean (Suriano & Sutton, 1981; Zdzitowiecki, 1992). The specimens of Lecithaster collected in the present study could not be assigned to any of those species, due to morphometric differences with the known species. The specimens are similar to those collected from O. nigricans and O. smitti in Nuevo and San José Gulfs, Chubut Province (Argentina), but the identification has not been determined (Carballo, 2008). The larva 3 of Cosmocephalus sp. most likely belongs to Cosmocephalus obvelatus (Creplin, 1825), since this species was recovered in the Chubut Province from O. nigricans parasitizing the same infection site (Carballo, Navone, et al., 2011). Four Cucullanus species have been described in the Argentinean Sea. Cucullanus marplatensisDaniel, Timi, and Sardella, 2002 was reported for Odontesthes species (Carballo, Laurenti, et al., 2011; Daniel et al., 2002). The Cucullanus specimens collected in this study differ from all the species of Cucullanus reported in Argentinean Sea. This finding would constitute a new parasite species. Peniculus fistula von Nordmann, 1832 was first recorded in the Strait of Magellan in an unknown host (Stuardo & Fagetti, 1961). Later, Peniculus sp. was registered in O. nigricans and O. smitti in the North Patagonian Gulfs (Carballo, Navone, et al., 2011). The specimens recovered in this work from O. nigricans, have a smaller length to width ratio (3.6-4.0) than P. fistula, which shows a trunk more than 6 times longer than wide (Alexander, 1983). They are similar to P. ostraciontis Yamaguti, 1939 and P. truncates Shiino, 1956 considering the distribution of swimming legs; however, our specimens cannot be assigned to any of these species since they have an intermediate length to width ratio of the trunk (P. truncatus 3.3 and P. ostraciontis 4.3) (Alexander, 1983).

For cultured O. bonariensis, the records herein correspond to the first reports of any parasites. The species richness of silversides collected from floating cages of Lacombe and Chascomús Pampean Lakes, were similar to those collected from wild silversides (Drago, 2012). Although richness was similar between cultured and wild specimens of Lacombe Pampean Lake the composition of the parasite community was different, for example T. cardiophilus and Argulus sp. were found only in cultured fish, and Hysterothylacium sp. and Wolffhuggelia matercula only in wild fish (Drago, 2012). This difference can be attributed to the life cycle of the parasites, meanwhile T. cardiophilus and Argulus sp. are transmitted by motile larvae (cercariae and juveniles), Hysterothylacium sp. and W. matercula require the consumption of an infected crustacean which are not available for cultured fishes. Silversides cultured in cages, which are located in the Pampean Lakes, acquired parasites from the environment, being of interest to human health Contracaecum sp., which is zoonotic, and for fish health Gyrodactylus sp. and Argulus sp., which could be pathogenic for fish if intensities of infection are increased (Woo, 1995).

Both freshwater silversides species were parasitized by the diplostomids A. mordax and T. cardiophilus, and were recorded in 6 new localities. Besides, Tylodelphys sp., T. destructor, T. barilochensis and Diplostomum sp. were recorded for O. hatcheri in 8 new localities. Both freshwater silversides species were parasitized by the heterophyids Ascocotyle sp. and Phagicola sp. constituting 4 new localities, and by the cestodes C. macdonaghi representing 7 new localities. Finally, the anisakid larvae Contracaecum sp., were found in O. bonariensis and O. hatcheri, while Hysterothylacium sp. was found only in O. hatcheri; these findings constitute 12 new localities. The following parasites: S. uruguayense (2 records), S. macrophallus (2), S. szidati (1), C. corderoi (5), A. tumescens (3), P. patagonicus (2), and D. chilensis (5) were recovered in new localities for O. hatcheri; and Gyrodactylus sp. (1) and Argulus sp. (1) represent new localities for O. bonariensis. The copepod E. sieboldi was first reported in Patagonia for Percichthys trucha (Cuvier & Valenciennes) (Szidat, 1956). Additionally larval stages and male specimens of E. sieboldi were reported from an Andean Patagonian lake (Modenutti & Balseiro, 1989). According to Szidat (1956), the Patagonian specimens showed scarce differences with specimens from Europe. Our specimens showed no differences with those collected from P. trucha from Pellegrini Lake and Limay River (Szidat, 1956). As the identity is dubious, we prefer to be conservative and assigned them to E. sieboldi, but molecular studies are needed to confirm the identity of the specimens.

The specimens of O. nigricans collected in this study showed a similar richness value (12 species) than those collected in Nuevo and San José gulfs (13 species in both gulfs). Although differences in the composition of parasite communities were observed, both populations share P. bartolii, Lecisthaster sp., Cosmocephalus sp., Hypoechinorhynchus sp., and Corynosoma sp., and differ in the presence of Diplostomum sp., Hysterothylacium sp., and C. rogercresseyi found in this study, and Prosorhynchoides sp., Huffmanela moraveci Carballo and Navone, 2007, Anisakis sp., Pseudoterranova sp., and Bomolochus globiceps (Vervoort and Ramírez, 1968) which were found only in the North Patagonian gulfs (Carballo, Navone, et al., 2011). These differences could be attributed to the fact that Nuevo and San José gulfs are in the ecotone between the Argentine and Patagonian ichthyogeographical provinces, while our samples were collected in Tierra del Fuego, in the southernmost part of Patagonian province. Although O. bonariensis and O. hatcheri were collected from 2 different ichthyogeographical provinces, Paranoplatensean Province and Patagonian Province, respectively; both share the metacercariae of A. mordax and T. cardiophilus and the cestode C. macdonaghi. The species of Odontesthes are mainly intermediate hosts for larval stages of Digenea and Nematoda, indicating that silversides in freshwater and marine environments are predominantly prey in the food chains.

Acknowledgements

To C. Luizon, G. Somoza, L. Miranda, and D. Collauti for their help in the collection of O. nigricans and O. bonariensis. We are grateful to Nahuel Huapi National Park authorities for sampling permissions. Financial support was provided by UNCo Grant (B-187), PIP 112-200801-01738 CONICET; and PICT BICENTENARIO N°1293 Agencia de Promoción Científica y Técnica.

References

Alexander, 1983 Alexander P.D. Peniculus haemuloni, a new species of copepod (Siphonostomatoida: Pennellidae) parasitic on Haemulon steindachneri from Ubatuba, Brazil. Bulletin of the British Museum (Natural History) Zoology. 1983; 45:381-5 [ Links ]

Carballo, 2008 Carballo M.C. Rol de los pejerreyes Odontesthes smitti y O. nigricans (Pisces: Atherinopsidae) como hospedadores de helmintos en los golfos Norpatagónicos, Chubut, Argentina. Ph.D. Dissertation. Argentina: Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata; 2008. [ Links ]

Carballo et al., 2012 Carballo M.C, Cremonte F, Navone G.T, Timi J.T. Similarity in parasite community structure may be used to trace latitudinal migrations of Odontesthes smitti along Argentinean coasts. Journal of Fish Biology. 2012; 80:15-28 [ Links ]

Carballo et al., 2011a Carballo M.C, Laurenti S, Cremonte F. A new species of monorchiid digenean from marine fishes in the Southwestern Atlantic Ocean off Patagonia. Systematic Parasitology. 2011; 78:233-40 [ Links ]

Carballo et al., 2011b Carballo M.C, Navone G.T, Cremonte F. Parasites of the silversides Odontesthes smitti and Odontesthes nigricans (Pisces: Atherinopsidae) from Argentinean Patagonia. Comparative Parasitology. 2011; 78:95-103 [ Links ]

Colautti et al., 2010 Colautti D.C, García J.R, Balboni L, Baigún C.R.M. Extensive cage culture of pejerrey (Odontesthes bonariensis) in a shallow pampean lake in Argentina. Aquaculture Research. 2010; 41:376-84 [ Links ]

Daniel et al., 2002 Daniel V.I, Timi J.T, Sardella N.H. Cucullanus marplatensis sp. nov. (Nematoda, Cucullanidae) parasitizing Odontesthes argentinensis (Valenciennes, 1835) (Pisces, Atherinidae) from Argentinean waters. Acta Parasitologica. 2002; 47:41-6 [ Links ]

Drago, 2012 Drago F.B. Community structure of metazoan parasites of silversides, Odontesthes bonariensis (Pisces, Atherinopsidae) from Argentina. Iheringia, Serie Zoologica. 2012; 102:26-32 [ Links ]

Dyer, 2000 Dyer B. Systematic review of the silverside fishes of Chile (Teleostei, Atheriniformes). Estudios Oceanológicos. 2000; 19:99-127 [ Links ]

Dyer, 2006 Dyer B. Systematic revision of the South American silversides (Teleostei, Atheriniformes). Biocell. 2006; 30:69-88 [ Links ]

González-Acuña et al., 2009 González-Acuña D, Cerda F, López J, Ortega R, Mathieu C, Kinsella M. Checklist of the helminths of the kelp gull, Larus dominicanus (Aves: Laridae) with new records from Chile. Zootaxa. 2009; 2297:27-43 [ Links ]

Grosman, 2001 Grosman F. Fundamentos biológicos, económicos y sociales para una correcta gestión del recurso pejerrey. Buenos Aires: Ed. Astyanax; 2001. [ Links ]

Lattuca et al., 2009 Lattuca M.E, Malanga G.F, Aguilar-Hurtado C, Pérez A.F, Calvo J, Puntarulo S. Main features of the oxidative metabolism in gills and liver of Odontesthes nigricans Richardson (Pisces, Atherinopsidae). Comparative Biochemistry and Physiology (B). 2009; 154:406-11 [ Links ]

Locke et al., 2015 Locke S.A, Al-Nasiri F.S, Caffara M, Drago F, Kalbe M, Lapierre A.R, et al. Diversity, specificity and speciation in larval Diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. International Journal of Parasitology. 2015; 45:841-55 [ Links ]

Mancini et al., 2006 Mancini M, Rodríguez C, Prosperi C, Salinas V, Bucco C. Main diseases of pejerrey (Odontesthes bonariensis) in central Argentina. Revista Pesquisa Veterinária Brasileira. 2006; 26:205-10 [ Links ]

Mancini et al., 2008 Mancini M, Bucco C, Salinas V, Larriestra A, Tanzola D, Guagliardo S. Seasonal variation of parasitism in pejerre y Odontesthes bonariensis (Atheriniformes, Atherinopsidae) from La Viña Reservoir (Córdoba, Argentina). Revista Brasileira de Parasitologia Veterinária. 2008; 17:22-38 [ Links ]

Modenutti and Balseiro, 1989 Modenutti B.E, Balseiro E.G. Presencia de Ergasilus sieboldi en el plancton de un lago Andino Argentino. Anales del Museo de Historia Natural de Valparaíso. 1989; 20:29-30 [ Links ]

Niewiadomska, 2002 Niewiadomska K. Family diplostomidae. In D. Gibson, A. Jones, & R. A. Bray (Eds.), Keys to the Trematoda (Vol. 1) London: CABI; 2002. 167-96 [ Links ]

Niewiadomska et al., 1989 Niewiadomska K, Zdzitowiecki K, Ostrowski-de Núñez M. Redescription of Diplostomum minutum Szidat, 1964 (Digenea, Diplostomidae). Acta Parasitologica Polonica. 1989; 34:267-71 [ Links ]

Ortubay et al., 1994 Ortubay S, Semenas L.G, Úbeda C.A, Quaggiotto A, Viozzi G. Catálogo de peces dulceacuícolas de la Patagonia Argentina y sus parásitos metazoos. Bariloche: Dirección de Pesca de la provincia de Río Negro; 1994. [ Links ]

Ruiz, 2007 Ruiz A.E. Biología del pejerrey patagónico en el Embalse Florentino Ameghino, Chubut, Argentina. Córdoba: Universitas; 2007. [ Links ]

Stuardo and Fagetti, 1961 Stuardo J, Fagetti E. Copépodos parásitos chilenos. I. Una lista de las especies conocidas y descripción de tres especies nuevas. Revista Chilena de Historia Natural. 1961; 55:55-82 [ Links ]

Suriano and Sutton, 1981 Suriano D.M, Sutton C.A. Contribución al conocimiento de la fauna parasitológica argentina VII. Digéneos de peces de la plataforma del Mar Argentino. Revista del Museo de La Plata (Nueva Serie). 1981; 124:261-71 [ Links ]

Szidat, 1956 Szidat L. Über die Parasitenfauna von Percichthys trucha (Cuv. & Val.) Girard der patagonischen Gewässer und die Beziehungen des Wirtsfisches und seiner Parasiten zur paläarktischen Region. Archiv für Hydrobiologie. 1956; 51:542-77 [ Links ]

Tanzola et al., 2009 Tanzola R.D, Semenas L, Viozzi G. Manejo y estado actual del conocimiento de los parásitos de peces cultivados en Argentina. In M. Tavares-Dias (Ed.), Manejo e Sanidade de Peixes em Cultivo. Amapá: Embrapa; 2009. 438-68 [ Links ]

Tombari and Volpedo, 2008 Tombari A, Volpedo A. Modificaciones en la distribución original de especies por impacto antrópico: el caso de Odontesthes bonariensis (Pisces: Atherinopsidae). In A. Volpedo, & L. Fernández Reyes (Eds.), Efecto de los cambios globales sobre la biodiversidad. Madrid: Programa Iberoamericano de Ciencias y Tecnología para el desarrollo; 2008. 155-65 [ Links ]

Woo, 1995 Woo P.T.K. Fish diseases and disorders. Vol. I. Protozoan and Metazoan infections. Cambridge: CAB International Press; 1995. [ Links ]

Zdzitowiecki, 1992 Zdzitowiecki K. Antarctic representatives of the genus Lecithaster Lühe, 1901 (Digenea, Hemiuridae), with the description of a new species. Acta Parasitologica. 1992; 37:57-63 [ Links ]

** Peer Review under the responsibility of Universidad Nacional Autónoma de México.

Received: September 26, 2014; Accepted: March 07, 2016

* Corresponding author. E-mail address: veronica.flores@crub.uncoma.edu.ar (V. Flores).

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License